Effects of Nosema ceranae and Lotmaria passim infections on honey bee foraging behaviour and physiology

Nosema ceranae and Lotmaria passim are two commonly encountered digestive tract parasites of the adult honey bee (Apis mellifera L.). Although these parasites are associated with colony losses, little is known about how they affect individual bee physiology and behaviour at the colony level. Using locally obtained isolates, we investigated the effects of both single and mixed infections of L. passim and N. ceranae on honey bee vitellogenin (Vg) expression and foraging behaviour. At the first instance of foraging, bees inoculated with either parasite had significantly lower Vg expression than uninoculated bees, with bees from the mixed infection treatment having the lowest Vg expression. Bees from the mixed infection treatment also had significantly higher densities of N. ceranae spores and numerically greater densities of L. passim cells per bee compared with bees inoculated with either parasite alone. In addition, bees from the mixed infection treatment had a significantly younger average foraging age compared with uninoculated bees from the same cohort. Although we did not find any effect of treatment on foraging effort, we discovered that bees inoculated with L. passim alone, or together with N. ceranae, had higher returning rates of foragers than control bees or bees inoculated with N. ceranae alone. Our findings indicate that both parasites can alter individual bee physiology, leading to individual changes in behaviour that could alter colony foraging dynamics. These have the potential to result in smaller, less productive colonies, decreased colony survivorship and reduced income for beekeepers.